Plant and Cell Physiology Advance Access originally published online on April 3, 2008
Plant and Cell Physiology 2008 49(5):835-842; doi:10.1093/pcp/pcn058
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CRR23/NdhL is a Subunit of the Chloroplast NAD(P)H Dehydrogenase Complex in Arabidopsis
1Graduate School of Agriculture, Kyushu University, Higashi-ku, Fukuoka, 812-8581 Japan
2Department of Botany, Graduate School of Science, Kyoto University, Sakyo-ku, Kyoto, 606-8502 Japan
3Plant Genomic Network Research Team, RIKEN Plant Science Center, Tsurumi-ku, Yokohama, 203-0045 Japan
4Faculty of Agriculture, University of Shizuoka, Suruga-ku, Shizuoka, 422-8529 Japan
*Corresponding author: E-mail, shikanai{at}pmg.bot.kyoto-u.ac.jp; Fax, +81-75-753-4257.
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Abstract |
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The chloroplast NAD(P)H dehydrogenase (NDH) complex functions in PSI cyclic and chlororespiratory electron transport in higher plants. Eleven plastid-encoded and three nuclear-encoded subunits have been identified so far, but the entire subunit composition, especially of the putative electron donor-binding module, is unclear. We isolated Arabidopsis thaliana crr23 (chlororespiratory reduction) mutants lacking NDH activity according to the absence of a transient increase in Chl fluorescence after actinic light illumination. Although CRR23 shows similarity to the NdhL subunit of cyanobacterial NDH-1, it has three transmembrane domains rather than the two in cyanobacterial NdhL. Unlike cyanobacterial NdhL, CRR23 is essential for stabilizing the NDH complex, which in turn is required for the accumulation of CRR23. Furthermore, CRR23 and NdhH, a subunit of chloroplast NDH, co-localized in blue-native gel. All the results indicate that CRR23 is an ortholog of cyanobacterial ndhL in Arabidopsis, despite its diversity of structure and function.
Keywords: Arabidopsis - Chloroplast - Cyclic electron transport - NAD(P)H dehydrogenase - Photosynthesis
Abbreviations: AL, actinic light; BN, blue native; crr, chlororespiratory reduction; DM, dodecyl maltoside; ETR, electron transport rate; NDH, NAD(P)H dehydrogenase; NPQ, non-photochemical quenching; PAM, pulse amplitude-modulated; PFD, photon flux density; PQ, plastoquinone; RT–PCR, reverse transcription–PCR.
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Introduction |
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The chloroplast NAD(P)H dehydrogenase (NDH) complex is homologous to NADH dehydrogenase (complex I) in mitochondria, and mediates PSI cyclic and chlororespiratory electron transport (Munekage and Shikanai 2005
, Rumeau et al. 2007, Shikanai 2007a, Shikanai 2007b). By analogy to mitochondrial and bacterial complexes, it is believed that chloroplast NDH mediates electron transport from stromal NAD(P)H to plastoquinone (PQ) in thylakoid membranes. On the basis of sequence similarity between subunits, chloroplast NDH is considered to have originated from cyanobacterial NDH-1 (Friedrich and Weiss 1997, Glynn et al. 2007; Shikanai 2007b). Cyanobacterial NDH-1 is involved in respiratory and PSI cyclic electron transport, and also in CO2 uptake by changing its subunit composition at the distal membrane domain (Battchikova and Aro 2007, Ogawa and Mi 2007).
Complex I in mammalian mitochondria consists of no fewer than 45 subunits (Carroll et al. 2002, Carroll et al. 2003, Janssen et al. 2006). In contrast, NDH-1 from Escherichia coli consists of a minimum set of only 14 subunits (two of the mitochondrial subunits are fused into one protein in E. coli), all of which are conserved in mitochondrial complex I (Leif et al. 1995, Yagi and Matsuno-Yagi 2003). Chloroplast NDH and cyanobacterial NDH-1 are more closely related to the E. coli NDH-1 complex than to the mitochondrial complex I. Out of the 14 subunits of E. coli NDH-1, 11 (NuoA–D, NuoH–N) are conserved in chloroplast NDH and cyanobacterial NDH-1 (NdhA–K) (Battchikova and Aro 2007, Shikanai 2007b). Homologs of NuoE–G, which function in NADH oxidization, are missing in chloroplast NDH and cyanobacterial NDH-1 even after searching the complete genome. This fact suggests that chloroplast NDH and cyanobacterial NDH-1 are equipped with different subunits functioning in electron donor binding. Recently, the putative entire complex containing the subcomplex corresponding to E. coli NuoE–G was captured by single-particle electron microscopy in cyanobacteria (Arteni et al. 2006). However, the proteins comprising this subcomplex have not been identified biochemically because of their low association (0.2%) with the core complex (Arteni et al. 2006). Thus, the electron donor-binding subunits of NDH involved in photosynthetic electron transport, and consequently also the electron donor to the NDH, are still unknown.
In addition to the 11 subunits common to higher plants and cyanobacteria, NdhL (renamed from IctA) was found to be essential to inorganic carbon transport in cyanobacteria, and was suggested to be one on the subunits of cyanobacterial NDH-1 (Ogawa 1991, Ogawa 1992). However, it took a long time until NdhL was shown to be an Ndh subunit, because of the difficulty of isolating the intact NDH-1 complex (Berger et al. 1993, Matsuo et al. 1998). A biochemical approach using mass spectrometry confirmed the existence of the subunits involved in CO2 uptake in cyanobacteria, but NdhL was still not detected (Herranen et al. 2004). Recently, novel subunits, NdhM and NdhN, were discovered in cyanobacterial NDH-1 (Prommeenate et al. 2004), and finally NdhL, as well as NdhO, was identified (Battchikova et al. 2005). NdhM–O were also identified in chloroplast NDH via partial purification of the complex (Rumeau et al. 2005). More recently, PsbP-like protein, PPL2, was suggested to be a subunit of chloroplast NDH (Ishihara et al. 2007).
Using the Chl fluorescence imaging technique, we identified Arabidopsis crr (chlororespiratory reduction) mutants specifically defective in chloroplast NDH activity (Hashimoto et al. 2003). In more exhaustive screening for crr mutants, we directly analyzed a series of mutant lines which have Ds transposons inserted in genes encoding putative plastid-targeting proteins by using pulse-amplitude-modulated (PAM) Chl fluorometry (Okuda et al. 2007). Here, we report the finding and characterization of Arabidopsis crr23 mutants. CRR23 is essential for the accumulation of the chloroplast NDH complex in Arabidopsis and is an Ndh subunit corresponding to cyanobacterial NdhL.
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Arabidopsis crr23 mutants are defective in NDH activity
The chloroplast NDH complex mediates electron donation from the stromal electron pool to PQ. NDH activity can be monitored as a transient increase in Chl fluorescence after the turning off of actinic light (AL) (Burrows et al. 1998
, Kofer et al. 1998, Shikanai et al. 1998). We focused on this fluorescence change to identify Arabidopsis crr mutants lacking NDH activity (Hashimoto et al. 2003). crr23-3 (ecotype Nössen) was isolated by screening of Ds transposon-tagged lines (Kuromori et al. 2004, Ito et al. 2005) by PAM fluorometry (Okuda et al. 2007). Fig. 1 shows a typical trace of the Chl fluorescence level in the wild type. crr23-3 was identified from its lack of a transient increase in fluorescence level after AL illumination, which indicates impaired NDH activity.
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CRR23 encodes cyanobacterial NdhL-like protein
In crr23-3, the At1g70760 gene was disrupted by a Ds insertion in the second intron (Fig. 2A). The crr23-3 defect has a recessive nature, and the phenotype was co-segregated with the Ds insertion (data not shown). In addition, we obtained crr23-1 (GABI-Kat 052F01), in which At1g70760 was disrupted by a T-DNA insertion in the second intron (Fig. 2A), and confirmed the lack of NDH activity by PAM Chl fluorometry (Fig. 1). Since the background of crr23-1 is Col, as in the other crr mutants (Hashimoto et al. 2003
), we used mainly this allele for further analysis. Reverse transcription–PCR (RT–PCR) analysis did not detect any mature At1g70760 transcripts in crr23-1 and crr23-3, indicating that both alleles are null (Fig. 2B). To verify that the crr23 phenotype is due to the disruption of At1g70760, we introduced a wild-type genomic sequence of At1g70760 into crr23-1. This complementation fully restored the transient increase in Chl fluorescence after AL illumination (Fig. 1). From these results, we conclude that the crr23 phenotype is due to the disruption of At1g70760.
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CRR23 (At1g70760) consists of five exons and four introns (Fig. 2A), and encodes a putative protein composed of 191 amino acids. TargetP 1.1 (http://www.cbs.dtu.dk/services/TargetP/) and ChloroP (http://www.cbs.dtu.dk/services/ChloroP/) predicted that the first 46 amino acids of CRR23 are the target signal to plastids. Three transmembrane domains were predicted in CRR23 by TMHMM v. 2.0 (http://www.cbs.dtu.dk/services/TMHMM-2.0/) (Fig. 2C). CRR23 has a weak similarity to cyanobacterial NdhL (Fig. 2C), as suggested by Battchikova et al. (2005
). Although cyanobacterial NdhL contains two transmembrane domains, CRR23 includes an additional one in the N-terminus (Fig. 2C). Proteins homologous to CRR23 were found in other plants and cyanobacteria (Fig. 2C), but not in non-phototrophs. Chlamydomonas reinhardtii, which lacks the chloroplast NDH complex (Peltier and Cournac 2002, Mus et al. 2005), does not contain a CRR23 homolog. Compared with the cyanobacterial NdhL, CRR23 has a short C-terminal extension. Except for the transmembrane domains, no known motifs that suggest the protein function were found in CRR23.
crr23 is specifically defective in the accumulation of chloroplast NDH
The absence of any Ndh subunit destabilizes the entire NDH complex (Horváth et al. 2000, Hashimoto et al. 2003, Zhang et al. 2004, Kotera et al. 2005, Rumeau et al. 2005). Exceptionally, however, the absence of the cyanobacterial NdhL does not destabilize the other subunits (Battchikova et al. 2005), although it drastically impairs the activity (Ogawa 1991, Ogawa 1992, Battchikova et al. 2005). To study the impact of the disruption of CRR23 on the stability of the NDH complex in Arabidopsis, we assessed the level of NdhH, a hydrophilic subunit of the NDH complex, in crr23-1 (Fig. 3). The NdhH level was drastically reduced to below the detection limit, at least to <12.5% of the wild-type level. It was fully restored by the introduction of the CRR23 genomic sequence (crr23-1 + CRR23). These results indicate that CRR23 is essential to stabilize the NDH complex in Arabidopsis.
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Since the contribution of the chloroplast NDH complex to photosynthetic electron transport is minor in Arabidopsis, mutants specifically defective in NDH activity do not show any distinct phenotype in seedlings grown at 50 µmol m–2 s–1 in a growth chamber (Hashimoto et al. 2003
, Muraoka et al. 2006, Shimizu et al. 2007). Also crr23 mutants exhibited no visible phenotype. To test whether the crr23 defect is specific to the NDH complex, we analyzed the light intensity dependence of two Chl fluorescence parameters, electron transport rate (ETR) and non-photochemical quenching (NPQ). ETR represents the rate of photosynthetic electron transport through PSII, and NPQ mainly reflects the dissipation of excess photo-energy as heat, which is regulated by monitoring the lumen pH (Krause and Weis 1991, Niyogi et al. 2005). These parameters reflect subtle defects in photosynthesis, and are therefore often used to characterize mutants defective in photosynthetic apparatus (Pogson et al. 1998, Munekage et al. 2002).
Neither ETR nor NPQ was affected in crr23-1 (Fig. 4). These results were consistent with the phenotype of other crr mutants specifically defective in NDH activity (Hashimoto et al. 2003, Munshi et al. 2006, Muraoka et al. 2006). From these results, we conclude that the accumulation of the NDH complex is specifically impaired in crr23.
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The NDH complex is essential for CRR23 accumulation
To characterize CRR23 protein, we raised an antibody against synthetic oligopeptides of CRR23, then conducted Western analysis of the chloroplast stromal fraction and the membrane fraction containing thylakoids and envelopes (Fig. 5). In the wild type, the antibody detected a protein of about 15 kDa in the membrane fraction, where the NDH complex localizes. This signal was not detected in crr23-1 but was detected in crr23-1 + CRR23, indicating that the antibody specifically detects CRR23. Localization of CRR23 in the membrane fraction is consistent with the presence of three transmembrane domains predicted by TMHMM. The molecular mass estimated by the mobility in the gel is slightly smaller than that predicted from the amino acid sequence (17 kDa). The transit peptide may be longer than the computer estimate. It is also possible that CRR23 (NdhL) migrates faster in the gel than the molecular marker proteins, as does cyanobacterial NdhL (Battchikova et al. 2005
).
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The level of NdhH was drastically reduced in crr23 (Fig. 3), indicating that CRR23 is essential for the accumulation of the NDH complex. This evidence, taken together with the sequence similarity (Fig. 2C), indicates that it is highly probable that CRR23 is an ortholog of cyanobacterial NdhL and a subunit of the chloroplast NDH complex. If this hypothesis is true, the absence of the NDH complex should lead to the degradation of CRR23. To assess this possibility, we analyzed the stability of CRR23 in the mutant backgrounds lacking the NDH complex (Fig. 5). crr2-2 is defective in ndhB expression owing to the lack of intergenic RNA cleavage between rps7 and ndhB in chloroplasts (Hashimoto et al. 2003
), and crr1-1 lacks a stromal protein, CRR1, which is essential for biogenesis or stabilization of the NDH complex, although its exact function remains unclear (Shimizu et al. 2007). In these mutants, the CRR23 level was reduced to about the detection limit. These results strongly suggest that CRR23 is one of the Ndh subunits, NdhL, in Arabidopsis.
CRR23 is the Arabidopsis NdhL subunit
To show further evidence that CRR23 is the Arabidopsis NdhL, we solubilized thylakoid membranes in 1% dodecyl maltoside (DM) and separated the protein complexes by blue-native (BN)/SDS two-dimensional PAGE. Separated proteins were blotted onto a membrane, and then NdhH and CRR23 were simultaneously detected by using the respective antibodies. We did not find any drastic differences in the two-dimensional PAGE patterns stained with Coomassie brilliant blue between the wild type and crr23-1 (Fig. 6B). In the wild type, the antibodies detected CRR23 and NdhH on the same vertical line corresponding to >1,000 kDa (estimated from the mobility of other complexes) in the BN gel (Fig. 6C), suggesting that these proteins were included in the same complex. The positions of CRR23 and NdhH in BN-PAGE were consistent with those of NdhH and NdhK reported by Aro et al. (2005). Spots corresponding to CRR23 and NdhH were not detected in crr23-1. We confirmed that the signals were always detected in the wild type but not in crr23-1 by repeating the experiments with two independently isolated thylakoids (data not shown). Taking all the results together, we conclude that CRR23 is NdhL in Arabidopsis.
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Discussion |
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In addition to 11 Ndh subunits encoded by the plastid genome, biochemical and genetic evidence indicates that three subunits, NdhM, NdhN and NdhO, are encoded by the nuclear genome in Arabidopsis (Rumeau et al. 2005
). Although the presence of a gene homologous to cyanobacterial ndhL was suggested (Battchikova et al. 2005), it has been unclear whether this gene really encodes the NDH subunit in chloroplasts on account of its low similarity to the cyanobacterial gene. Here, we show that CRR23 was essential for stabilizing the NDH complex (Fig. 3), and the NDH complex was required for the accumulation of CRR23 (Fig. 5). CRR23 localized to the thylakoid membranes (Fig. 5) and co-migrated with NdhH in the BN gel (Fig. 6). The phenotype of the crr23 knockouts was specific to the loss of NDH (Figs. 1, 4). From these results, we conclude that CRR23 is an ortholog of the cyanobacterial ndhL and rename it Arabidopsis ndhL.
Predicted mature NdhL and its putative orthologs in other higher plants have extensions in both the N- and C-termini compared with cyanobacterial NdhL (Fig. 2C, Battchikova et al. 2005). The N-terminal extension was predicted to be a transmembrane domain, suggesting that chloroplast NdhL has three transmembrane domains rather than the two in cyanobacteria. The presence of the additional domain may be required for the function of NdhL in chloroplasts, which is divergent from that of cyanobacterial NdhL. Although NdhL is not essential for stabilizing the NDH complex in cyanobacteria (Battchikova et al. 2005), the chloroplast NDH complex is unstable in the absence of NdhL. Alternatively, the additional transmembrane domain may interact with other Ndh membrane subunits or a factor specific to the chloroplast complex, such as CRR3 (Muraoka et al. 2006).
In contrast to the hydrophobic N-terminal extension, the C-terminal extension is hydrophilic. Since the C-terminal sequence is not well conserved among higher plants (Fig. 2C), it may not be essential for function. Consistent with this idea, Arabidopsis crr23-2, in which the C-terminal 25 amino acids of NdhL are truncated by a T-DNA insertion, retained a trace of NDH activity (data not shown).
Recently, the existence of two forms of the NDH complex, monomeric (550 kDa) and dimeric (1,000–1,100 kDa), in Zea mays was reported (Darie et al. 2005). More recently, a similar result was reported in Arabidopsis (Ishihara et al. 2007). In our result, however, Ndh subunits were detected only in a single line of spots corresponding to a molecular mass of >1,000 kDa (Fig. 6), which is consistent with the result of Aro et al. (2005). This line of spots would correspond to dimeric NDH (Darie et al. 2005). The detection of the monomeric form seems to be dependent on the experimental conditions, such as concentration or type of detergent. Ndh subunits were detected in tobacco in complexes of 550 and 
200 kDa when a high concentration of DM (2.5%) was used (Burrows et al. 1998). It seems essential to use milder conditions for solubilization, such as 1% DM (Fig. 6, Aro et al. 2005) or 1.5% digitonin (Heinemeyer et al. 2004), to detect the larger complex.
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Materials and Methods |
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Plant materials and growth conditions
Arabidopsis thaliana (ecotype Columbia gl1, Columbia-0 or Nössen) was grown in soil in a growth chamber [photon flux density (PFD) of 50 µmol photons m–2 s–1, 16 h photoperiod, 23°C] for 3–4 weeks. crr23-3 was mutagenized by Ds transposon insertion (Kuromori et al. 2004
, Ito et al. 2005). crr23-1, the T-DNA insertion mutant line 052F01, was provided by GABI-Kat (http://www.gabi-kat.de). The ecotype of crr23-1 was changed from Columbia-0 to Columbia gl1 by backcrossing with Columbia gl1 followed by screening of F2 plants.
Chl fluorescence analysis
Chl fluorescence was measured with a MINI-PAM portable Chl fluorometer (Walz, Effeltrich, Germany) in ambient air at room temperature (25°C). Minimum fluorescence at open PSII centers in the dark-adapted state (Fo) was excited by a weak measuring light (wavelength 650 nm) at a PFD of 0.05–0.1 µmol m–2 s–1. A saturating pulse of white light (800 ms, 3,000 µmol photons m–2 s–1) was applied to determine the maximum fluorescence at closed PSII centers in the dark-adapted state (Fm) and during AL illumination (Fm'). The steady-state fluorescence level (Fs) was recorded during AL illumination (15–1,000 µmol photons m–2 s–1). These photosynthetic parameters were determined 2 min after the change of AL intensity. NPQ was calculated as (Fm – Fm')/Fm'. The quantum yield of PSII (
PSII) was calculated as (Fm' – Fs)/Fm' (Genty et al. 1989). ETR was calculated as PSIIxPFD. The transient increase in Chl fluorescence after AL had been turned off was monitored as described (Shikanai et al. 1998).
RT–PCR analysis
Total RNA was prepared from Arabidopsis leaves and roots by using an RNeasy Plant Mini Kit (Qiagen, http://www1.qiagen.com/). Total RNA (2 µg) was reverse-transcribed with oligo d(T)20 in a SuperScript III First-Strand Synthesis System for RT–PCR (Invitrogen, http://www.invitrogen.com/) in a total volume of 20 µl. cDNA was used in a subsequent PCR with KOD Plus (Toyobo, http://www.toyobo.co.jp/). PCR primers used were 5'-CTTGAAGCCACGCAGTGTCAAATC-3' and 5'-CTCTTAGCCAGTTCATGATGATTGG-3' for CRR23, and 5'-GAGAGATTCAGGTGCCCAG-3' and 5'-AGAGCGAGAGCGGGTTTTCA-3' for ACT8. Each set of primers covered at least one intron sequence to distinguish amplification of cDNA from genomic DNA. RT–PCR products were separated through an agarose gel and detected by ethidium bromide staining. The number of cycles was optimized so that the abundance of products could be compared within the linear phase of amplification.
Protein blot analysis
Chloroplasts were isolated as described (Munekage et al. 2002). Chloroplasts were burst by suspension in 20 mM HEPES/KOH (pH 7.6), 5 mM MgCl2 and 2.5 mM EDTA, and centrifuged at 7,700xg for 3 min to separate the stromal fraction (supernatant) from the fraction containing the thylakoid membranes and chloroplast envelopes (precipitate). Proteins were separated by 15% SDS–PAGE (for CRR23) or 12.5% SDS–PAGE (for the others), transferred to a nitrocellulose membrane (for NdhH) or a polyvinylidene difluoride membrane (for the others), and detected with an ECL Advance Western Blotting Detection Kit (for NdhH) or an ECL Plus Western Blotting Detection Kit (for the others) (GE Healthcare, http://www.gehealthcare.com/). CRR23 was detected with rabbit polyclonal antibody prepared against C+RDPNMKNPWDKPTD and C+LKYPYATPEDYDLD conjugated with keyhole limpet hemocyanin (Operon Biotechnologies, https://www.operon.com/).
Two-dimensional PAGE analysis
BN-PAGE was performed as described (Peng et al. 2006) with a few modifications. The fresh thylakoid membranes were washed twice in 25BTH20G buffer (25 mM BisTris–HCl, pH 7.0, 20% glycerol) and suspended in solubilization buffer (25 mM BisTris–HCl, pH 7.0, 20% glycerol, 1% DM) at 1 µg Chl µl–1. After incubation on ice for 10 min, insoluble material was removed by centrifugation at 12,000xg for 10 min. Solubilized membranes were mixed with one-tenth volume of BN sample buffer (100 mM BisTris–HCl, pH 7.0, 5% Serva blue G, 0.5 M 6-amino-n-caproic acid, 30% sucrose) and separated by 0.75 mm thick 5–12% gradient BN-PAGE. For 2D analysis, excised BN-PAGE lanes were soaked in SDS sample buffer containing 2.5% β-mercaptoethanol for 30 min and layered onto 1 mm thick 15% SDS–polyacrylamide gels. After electrophoresis, the proteins were stained by Coomassie brilliant blue or transferred to nitrocellulose membranes and detected with an ECL Advance Western Blotting Detection Kit.
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Japan Society for the Promotion of Science (JSPS) grant-in-aid for Creative Scientific Research (17GS0316 to T.S.), Ministry of Education, Culture, Sports, Science and Technology of Japan Scientific Research on Priority Areas (16085206 to T.S.); JSPS (19-07142 to L.P.).
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We thank Misato Tanoue and Asako Tahara for their skilled technical support. We are grateful to Gilles Peltier, Tsuyoshi Endo, Amane Makino and Akiho Yokota for their gifts of antibodies.
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(Received February 29, 2008; Accepted April 1, 2008)
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